Citrullinated peptide dendritic cell immunotherapy in HLA risk genotype-positive rheumatoid arthritis patients

Science Translational Medicine

Volumn 7, Issue 290, 2015, Pages

  Benham, Helen ^a   Nel, Hendrik J ^a   Law, Soi Cheng ^a   Mehdi, Ahmed M ^a   Street, Shayna ^a   Ramnoruth, Nishta ^a   Pahau, Helen ^a   Lee, Bernett T ^b   Ng, Jennifer ^a   Brunck, Marion E G ^a   Hyde, Claire ^a   Trouw, Leendert A ^c   Dudek, Nadine L ^d   Purcell, Anthony W ^d   O'Sullivan, Brendan J ^a   Connolly, John E ^b   Paul, Sanjoy K ^a,e   Lê Cao, Kim Anh ^a   Thomas, Ranjeny ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b AGENCY FOR SCIENCE   (Singapore)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d MONASH UNIVERSITY   (Australia)

^e QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; CXCL11 CHEMOKINE; CYCLIC CITRULLINATED PEPTIDE ANTIBODY; FRACTALKINE; HLA DRB1 ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 29; INTERLEUKIN 6; RHEUMAVAX; UNCLASSIFIED DRUG; VIMENTIN; CITRULLINE; HLA ANTIGEN; PEPTIDE;

ADULT; ALLERGY; ANAPHYLAXIS; ANEMIA; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DISEASE ACTIVITY; DISEASE EXACERBATION; DISEASE SEVERITY; DRUG ACTIVITY; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG MEGADOSE; DRUG SAFETY; DRUG TOLERABILITY; EFFECTOR CELL; EXPLORATORY RESEARCH; FEMALE; GENETIC RISK; GENOTYPE; HEADACHE; HUMAN; HUMAN CELL; HYPOGLYCEMIA; IMMUNOTHERAPY; INJECTION SITE REACTION; LEUKOPENIA; LOW DRUG DOSE; LYMPHADENOPATHY; LYMPHOCYTOPENIA; MALE; NEUTROPENIA; OPEN STUDY; PHASE 1 CLINICAL TRIAL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; SIDE EFFECT; SINGLE DRUG DOSE; AGED; ARTHRITIS, RHEUMATOID; CHEMISTRY; GENETICS; IMMUNOLOGY; MIDDLE AGED;

AGED; ARTHRITIS, RHEUMATOID; CITRULLINE; DENDRITIC CELLS; FEMALE; HLA ANTIGENS; HUMANS; IMMUNOTHERAPY; MALE; MIDDLE AGED; PEPTIDES;

EID: 84930453993     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaa9301     Document Type: Article

References (51)

1. D. L. Scott, F. Wolfe, T. W. Huizinga, Rheumatoid arthritis. Lancet 376, 1094-1108 (2010).
2. M. F. Bakker, J. W. Jacobs, S. M. Verstappen, J. W. Bijlsma, Tight control in the treatment of rheumatoid arthritis: Efficacy and feasibility. Ann. Rheum. Dis. 66 (Suppl. 3), iii56-iii60 (2007).
3. R. Thomas, Dendritic cells and the promise of antigen-specific therapy in rheumatoid arthritis. Arthritis Res. Ther. 15, 204 (2013).
4. C. Daniel, H. Ploegh, H. von Boehmer, Antigen-specific induction of regulatory T cells in vivo and in vitro. Methods Mol. Biol. 707, 173-185 (2011).
5. J. Idoyaga, C. Fiorese, L. Zbytnuik, A. Lubkin, J. Miller, B. Malissen, D. Mucida, M. Merad, R. M. Steinman, Specialized role of migratory dendritic cells in peripheral tolerance induction. J. Clin. Invest. 123, 844-854 (2013).
6. E. C. Koffeman, M. Genovese, D. Amox, E. Keogh, E. Santana, E. L. Matteson, A. Kavanaugh, J. A. Molitor, M. H. Schiff, J. O. Posever, J. M. Bathon, A. J. Kivitz, R. Samodal, F. Belardi, C. Dennehey, T. van den Broek, F. van Wijk, X. Zhang, P. Zieseniss, T. Le, B. A. Prakken, G. C. Cutter, S. Albani, Epitope-specific immunotherapy of rheumatoid arthritis: Clinical responsiveness occurs with immune deviation and relies on the expression of a cluster of molecules associated with T cell tolerance in a double-blind, placebo-controlled, pilot phase II trial. Arthritis Rheum. 60, 3207-3216 (2009).
7. A. Kavanaugh, M. Genovese, J. Baughman, A. Kivitz, K. Bulpitt, N. Olsen, M. Weisman, E. Matteson, D. Furst, R. van Vollenhoven, J. Anderson, S. Cohen, N. Wei, J. Meijerink, C. Jacobs, S. Mocci, Allele and antigen-specific treatment of rheumatoid arthritis: A double blind, placebo controlled phase 1 trial. J. Rheumatol. 30, 449-454 (2003).
8. D. E. Trentham, R. A. Dynesius-Trentham, E. J. Orav, D. Combitchi, C. Lorenzo, K. L. Sewell, D. A. Hafler, H. L. Weiner, Effects of oral administration of type II collagen on rheumatoid arthritis. Science 261, 1727-1730 (1993).
9. J. Banchereau, F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, K. Palucka, Immunobiology of dendritic cells. Annu. Rev. Immunol. 18, 767-811 (2000).
10. L. M. van Duivenvoorde, P. Louis-Plence, F. Apparailly, E. I. van der Voort, T. W. Huizinga, C. Jorgensen, R. E. Toes, Antigen-specific immunomodulation of collagen-induced arthritis with tumor necrosis factor-stimulated dendritic cells. Arthritis Rheum. 50, 3354-3364 (2004).
11. E. Martin, C. Capini, E. Duggan, V. P. Lutzky, P. Stumbles, A. R. Pettit, B. O'Sullivan, R. Thomas, Antigen-specific suppression of established arthritis in mice by dendritic cells deficient in NF-κB. Arthritis Rheum. 56, 2255-2266 (2007).
12. J. N. Stoop, R. A. Harry, A. von Delwig, J. D. Isaacs, J. H. Robinson, C. M. Hilkens, Therapeutic effect of tolerogenic dendritic cells in established collagen-induced arthritis is associated with a reduction in Th17 responses. Arthritis Rheum. 62, 3656-3665 (2010).
13. P. K. Gregersen, J. Silver, R. J. Winchester, The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 30, 1205-1213 (1987).
14. S. Viatte, D. Plant, S. Raychaudhuri, Genetics and epigenetics of rheumatoid arthritis. Nat. Rev. Rheumatol. 9, 141-153 (2013).
15. L. Klareskog, A. I. Catrina, S. Paget, Rheumatoid arthritis. Lancet 373, 659-672 (2009).
16. M. van Oosterhout, I. Bajema, E. W. Levarht, R. E. Toes, T. W. Huizinga, J. M. van Laar, Differences in synovial tissue infiltrates between anti-cyclic citrullinated peptide-positive rheumatoid arthritis and anti-cyclic citrullinated peptide-negative rheumatoid arthritis. Arthritis Rheum. 58, 53-60 (2008).
17. J. A. Hill, S. Southwood, A. Sette, A. M. Jevnikar, D. A. Bell, E. Cairns, Cutting edge: The conversion of arginine to citrulline allows for a high-affinity peptide interaction with the rheumatoid arthritis-associated HLA-DRB1∗0401 MHC class II molecule. J. Immunol. 171, 538-541 (2003).
18. S. C. Law, S. Street, C. H. Yu, C. Capini, S. Ramnoruth, H. J. Nel, E. van Gorp, C. Hyde, K. Lau, H. Pahau, A. W. Purcell, R. Thomas, T-cell autoreactivity to citrullinated autoantigenic peptides in rheumatoid arthritis patients carrying HLA-DRB1 shared epitope alleles. Arthritis Res. Ther. 14, R118 (2012).
19. A. von Delwig, J. Locke, J. H. Robinson, W. F. Ng, Response of Th17 cells to a citrullinated arthritogenic aggrecan peptide in patients with rheumatoid arthritis. Arthritis Rheum. 62, 143-149 (2010).
20. S. W. Scally, J. Petersen, S. C. Law, N. L. Dudek, H. J. Nel, K. L. Loh, L. C. Wijeyewickrema, S. B. Eckle, J. van Heemst, R. N. Pike, J. McCluskey, R. E. Toes, N. L. La Gruta, A. W. Purcell, H. H. Reid, R. Thomas, J. Rossjohn, A molecular basis for the association of the HLA-DRB1 locus, citrullination, and rheumatoid arthritis. J. Exp. Med. 210, 2569-2582 (2013).
21. E. James, M. Rieck, J. Pieper, J. A. Gebe, B. B. Yue, M. Tatum, M. Peda, C. Sandin, L. Klareskog, V. Malmstrom, J. H. Buckner, Citrulline-specific Th1 cells are increased in rheumatoid arthritis and their frequency is influenced by disease duration and therapy. Arthritis Rheumatol. 66, 1712-1722 (2014).
22. B. J. O'Sullivan, R. Thomas, CD40 ligation conditions dendritic cell antigen-presenting function through sustained activation of NF-κB. J. Immunol. 168, 5491-5498 (2002).
23. D. Diogo, Y. Okada, R. M. Plenge, Genome-wide association studies to advance our understanding of critical cell types and pathways in rheumatoid arthritis: Recent findings and challenges. Curr. Opin. Rheumatol. 26, 85-92 (2014).
24. A. R. Pettit, K. P. MacDonald, B. O'Sullivan, R. Thomas, Differentiated dendritic cells expressing nuclear RelB are predominantly located in rheumatoid synovial tissue perivascular mononuclear cell aggregates. Arthritis Rheum. 43, 791-800 (2000).
25. M. L. Handel, L. B. McMorrow, E. M. Gravallese, Nuclear factor-κB in rheumatoid synovium. Localization of p50 and p65. Arthritis Rheum. 38, 1762-1770 (1995).
26. E. Martin, B. O'Sullivan, P. Low, R. Thomas, Antigen-specific suppression of a primed immune response by dendritic cells mediated by regulatory T cells secreting interleukin-10. Immunity 18, 155-167 (2003).
27. M. Li, X. Zhang, X. Zheng, D. Lian, Z. X. Zhang, W. Ge, J. Yang, C. Vladau, M. Suzuki, D. Chen, R. Zhong, B. Garcia, A. M. Jevnikar, W. P. Min, Immune modulation and tolerance induction by RelB-silenced dendritic cells through RNA interference. J. Immunol. 178, 5480-5487 (2007).
28. - dendritic cells are sensitized not anergic to subsequent activation. J. Immunol. 173, 1671-1680 (2004).
29. D. White, H. Pahau, E. Duggan, S. Paul, R. Thomas, Trajectory of intensive treat-to-target disease modifying drug regimen in an observational study of an early rheumatoid arthritis cohort. BMJ Open 3, e003083 (2013).
30. D. E. Smilek, M. R. Ehlers, G. T. Nepom, Restoring the balance: Immunotherapeutic combinations for autoimmune disease. Dis. Model. Mech. 7, 503-513 (2014).
31. P. M. Brown, J. D. Isaacs, Rheumatoid arthritis: From palliation to remission in two decades. Clin. Med. 14 (Suppl. 6), s50-s55 (2014).
32. M. A. Rank, D. I. Bernstein, Improving the safety of immunotherapy. J. Allergy Clin. Immunol. Pract. 2, 131-135 (2014).
33. B. M. Smithers, K. O'Connell, S. MacFadyen, M. Chambers, K. Greenwood, A. Boyce, I. A. Jabbar, K. Barker, K. Grimmett, E. Walpole, R. Thomas, Clinical response after intradermal immature dendritic cell vaccination in metastatic melanoma is associated with immune response to particulate antigen. Cancer Immunol. Immunother. 52, 41-52 (2003).
34. 111In-labeled dendritic cell human vaccines improved by reducing number of cells. Clin. Cancer Res. 19, 1525-1533 (2013).
35. R. Thomas, M. Chambers, R. Boytar, K. Barker, L. L. Cavanagh, S. MacFadyen, B. M. Smithers, M. Jenkins, J. Andersen, Immature human monocyte-derived dendritic cells migrate rapidly to draining lymph nodes after intradermal injection for melanoma immunotherapy. Melanoma Res. 9, 474-481 (1999).
36. O. Boyman, C. Krieg, D. Homann, J. Sprent, Homeostatic maintenance of T cells and natural killer cells. Cell. Mol. Life Sci. 69, 1597-1608 (2012).
37. D. L. Asquith, I. B. McInnes, Emerging cytokine targets in rheumatoid arthritis. Curr. Opin. Rheumatol. 19, 246-251 (2007).
38. P. Deshpande, M. M. Cavanagh, S. Le Saux, K. Singh, C. M. Weyand, J. J. Goronzy, IL-7- and IL-15-mediated TCR sensitization enables T cell responses to self-antigens. J. Immunol. 190, 1416-1423 (2013).
39. Y. Zheng, S. Josefowicz, A. Chaudhry, X. P. Peng, K. Forbush, A. Y. Rudensky, Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 463, 808-812 (2010).
40. Z. Chen, J. Barbi, S. Bu, H. Y. Yang, Z. Li, Y. Gao, D. Jinasena, J. Fu, F. Lin, C. Chen, J. Zhang, N. Yu, X. Li, Z. Shan, J. Nie, Z. Gao, H. Tian, Y. Li, Z. Yao, Y. Zheng, B. V. Park, Z. Pan, J. Zhang, E. Dang, Z. Li, H. Wang, W. Luo, L. Li, G. L. Semenza, S. G. Zheng, K. Loser, A. Tsun, M. I. Greene, D. M. Pardoll, F. Pan, B. Li, The ubiquitin ligase Stub1 negatively modulates regulatory T cell suppressive activity by promoting degradation of the transcription factor Foxp3. Immunity 39, 272-285 (2013).
41. A. P. Cope, R. S. Liblau, X. D. Yang, M. Congia, C. Laudanna, R. D. Schreiber, L. Probert, G. Kollias, H. O. McDevitt, Chronic tumor necrosis factor alters T cell responses by attenuating T cell receptor signaling. J. Exp. Med. 185, 1573-1584 (1997).
42. M. R. Ehrenstein, J. G. Evans, A. Singh, S. Moore, G. Warnes, D. A. Isenberg, C. Mauri, Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFα therapy. J. Exp. Med. 200, 277-285 (2004).
43. T. Odai, M. Matsunawa, R. Takahashi, K. Wakabayashi, T. Isozaki, N. Yajima, Y. Miwa, T. Kasama, Correlation of CX3CL1 and CX3CR1 levels with response to infliximab therapy in patients with rheumatoid arthritis. J. Rheumatol. 36, 1158-1165 (2009).
44. B. R. Burton, G. J. Britton, H. Fang, J. Verhagen, B. Smithers, C. A. Sabatos-Peyton, L. J. Carney, J. Gough, S. Strobel, D. C. Wraith, Sequential transcriptional changes dictate safe and effective antigen-specific immunotherapy. Nat. Commun. 5, 4741 (2014).
45. S. C. Law, H. Benham, H. H. Reid, J. Rossjohn, R. Thomas, Identification of self-antigen-specific T cells reflecting loss of tolerance in autoimmune disease underpins preventative immunotherapeutic strategies in rheumatoid arthritis. Rheum. Dis. Clin. North Am. 40, 735-752 (2014).
46. K. N. Henderson, J. A. Tye-Din, H. H. Reid, Z. Chen, N. A. Borg, T. Beissbarth, A. Tatham, S. I. Mannering, A. W. Purcell, N. L. Dudek, D. A. van Heel, J. McCluskey, J. Rossjohn, R. P. Anderson, A structural and immunological basis for the role of human leukocyte antigen DQ8 in celiac disease. Immunity 27, 23-34 (2007).
47. S. Edupuganti, R. B. Eidex, H. Keyserling, R. S. Akondy, R. Lanciotti, W. Orenstein, C. del Rio, Y. Pan, T. Querec, H. Lipman, A. Barrett, R. Ahmed, D. Teuwen, M. Cetron, M. J. Mulligan; YF-Ig Study Team, A randomized, double-blind, controlled trial of the 17D yellow fever virus vaccine given in combination with immune globulin or placebo: Comparative viremia and immunogenicity. Am. J. Trop. Med. Hyg. 88, 172-177 (2013).
48. A. Willemze, D. van der Woude, W. Ghidey, E. W. Levarht, G. Stoeken-Rijsbergen, W. Verduyn, R. R. de Vries, J. J. Houwing-Duistermaat, T. W. Huizinga, L. A. Trouw, R. E. Toes, The interaction between HLA shared epitope alleles and smoking and its contribution to autoimmunity against several citrullinated antigens. Arthritis Rheum. 63, 1823-1832 (2011).
49. G. Boire, P. Cossette, A. J. de Brum-Fernandes, P. Liang, T. Niyonsenga, Z. J. Zhou, N. Carrier, C. Daniel, H. A. Menard, Anti-Sa antibodies and antibodies against cyclic citrullinated peptide are not equivalent as predictors of severe outcomes in patients with recent-onset polyarthritis. Arthritis Res. Ther. 7, R592-R603 (2005).
50. D. Saadoun, M. Rosenzwajg, F. Joly, A. Six, F. Carrat, V. Thibault, D. Sene, P. Cacoub, D. Klatzmann, Regulatory T-cell responses to low-dose interleukin-2 in HCV-induced vasculitis. N. Engl. J. Med. 365, 2067-2077 (2011).
51. H. Wold, Estimation of principal component and related models by iterative least squares, in Multivariate Analysis (Academic Press, New York, 1966), pp. 391-420.